Arq Neuropsiquiatr 2005;63(2-A):339-344

CLIP READJUSTMENT IN ANEURYSM SURGERY
AFTER FLOW EVALUATION USING THE
ULTRASONIC PERIVASCULAR PROBE
Case report
Walter J. Fagundes-Pereyra, William E. Hoffman, Mukesh Misra, Fady T. Charbel
ABSTRACT - Occlusion or stenosis of a parent vessel or its distal branches is a major cause of poor patient
outcome after cerebral aneurysm surgery. Despite great attempts to preserve patency at the time of clip
application, intraoperative visual observation may not reveal arterial compromise or occlusion. Quantitative
measurement of blood flow in cerebral vessels during aneurysm surgery can help prevent ischaemia and
improve patient outcome. We report a case of a large complex middle cerebral artery (MCA) aneurysm in
which perivascular microflow probes were used to measure blood flow quantitatively in MCA and its branches before and after aneurysm clipping. Following aneurysm clipping, blood flow in the MCA branches were
significantly reduced to less than its initial baseline value with occlusion of the inferior M2 segment. Prompt
detection of compromised blood flow gave the surgeon the opportunity to adjust the clip. This adjustment was performed several times until restore MCA flow to its preclipping values. Intraoperative quantitative vessel-flow measurements were safe and may have prevented cerebral ischaemia and neurological deficit
to this patient.
KEY WORDS: ultrasonic perivascular transit-time flow probe, aneurysm surgery, middle cerebral artery.

Reajuste do clipe na cirurgia de aneurisma após avaliação do fluxo arterial por meio de microsonda ultrasônica perivascular: relato de caso
RESUMO - A medida quantitativa do fluxo sanguíneo nos vasos cerebrais durante a cirurgia de aneurisma
pode ajudar na prevenção de eventos isquêmicos e, portanto, melhorar os resultados. Relatamos o caso de
paciente portador de aneurisma grande e complexo da bifurcação da artéria de cerebral média (ACM), no
qual foram usadas micro-sondas ultrasônicas perivasculares para medir o fluxo de sangue quantitativamente
na ACM e nos seus ramos antes e depois da clipagem do aneurisma. Após a clipagem do aneurisma, o fluxo
de sangue diminuiu em todos os ramos, fazendo-se necessário o reajuste do clipe. Após vários ajustes na posição do clipe, o fluxo sanguíneo nos segmentos da ACM foi restabelecido. A descoberta imediata da alteração do fluxo de sangue proporcionou a oportunidade ao cirurgião de ajuste do clipe e conseqüentemente o restabelecimento do fluxo a valores compatíveis àqueles antes da clipagem. O uso de micro-sondas ultrasônicas perivasculares para medida do fluxo sanguíneo durante a cirurgia de aneurisma pode prevenir eventos isquêmicos e eventualmente déficits neurológicos.
PALAVRAS-CHAVE: micro-sonda ultrasônica perivascular, fluxo sanguíneo, aneurisma, artéria cerebral média.

The outcome of surgical treatment of cerebral
aneurysms may be severely impaired by local ischaemia, or by infarction resulting from the inadvertent
occlusion or stenosis of a parent vessel or its distal
branches1-4. Incomplete aneurym occlusion, on the
other hand, increases the risk of haemorrhage. Despite great attempts to preserve patency at the time
of clip application, intraoperative visual observation
may not reveal arterial compromise or occlusion1.

Angiographic data provided in the literature indicate that an intraoperative method of measuring cerebral vessel flow during aneurysm surgery would enable early detection of compromised flow and may
reduce the risk of permanent neurological deficit5-7.
In this report we describe the use of a ultrasonic perivascular microflow probe for quantitative vessel-flow measurement during middle cerebral artery
(MCA) bifurcation aneurysm surgery. This technique

Department of Neurosurgery, University of Illinois at Chicago, USA 912 South Wood St. Chicago, Illinois 60612.
Received 21 June 2004, received in final form 19 September 2004. Accepted 10 November 2004.
Dr. Walter J. Fagundes-Pereyra - Rua Walter José Pasolini 100 - 29050-490 Vitória ES - Brasil. E-mail: walter@neurocirurgia.com

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Fig 1. Computed tomography scan demostrating a subarachnoid hemorrhage grade IV in the right sylvian fissure
and left ventricular cateter (A). Oblique right ICA angiogram revealing a large right MCA bifurcation aneurysm (B).

Fig 2. Lateral right ICA angiogram performed immediatly after embolization demonstrating apparent complete occlusion of the aneurysm (A), two weeks later demonstrating a partial recanalization of the posterior
chamber of the MCA aneurysm (B).

permits immediate evaluating of vessel-flow during
aneurysm clipping and the ability to repeated measurements if multiple clip adjustments are needed.
CASE
A 42-year-old right handed Caucasian man presented with headache, nausea and seizures. Two days prior to

admission, the headache worsened. A computed tomography (CT) scan study demonstrated a subarachnoid hemorrhage in the right sylvian cistern, grade IV of Fisher
(Fig 1A). In addition, there was an intraparenchymal hemorrhage involving the right temporal lobe. The patient
was transferred to the University of Illinois at Chicago Medical Center for further evaluation and management.

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Fig 3. Schematic diagram showing a MCA aneurysm and two branches arising from the bifurcation of MCA with one branch
very close to the neck of the aneurysm.

Fig 4. Schematic diagram showing flow probe on the M2 segment (A) and intraoperative tracings before (superior trace) and after
(middle trace) clipping, and the final (inferior trace) mean blood flow (ml/min) after multiple clip readjustment (B).

Cerebral angiography revealed a large right MCA
bifurcation aneurysm measuring 15 X 8 mm (Fig 1B). The
aneurysm was thought to be sucessfully coiled (Fig 2A).
Subsequent cerebral angiography revealed partial recanalization of the posterior chamber of the aneurysm (Fig
2B) and moderate vasospasm involving the right carotid
artery and M1 segment of the right MCA.
The patient was surgically treated four weeks after
coil embolization for aneurysm clipping. The aneurysm
was approached through a right side pterional craniotomy. The aneurysm was found to be large and partially
packed with coils and thrombus. The MCA was identified
as its two branches (here referred as M1 and superior and
inferior M2 segments) arising from its bifurcation, with
one branch very close to the neck of the aneurysm (Fig
3). Once all branches arising from the bifurcation of MCA

were dissected free, a cerebral protection was performed,
and a temporarily clip was applied to the MCA and to the
two other branches. The aneurysm was then completely dissected and an incision was made on the surface and
the coils and thrombus were carefully removed from the
aneurysm. Once the aneurysm coils were delivered, the
lumen of the aneurysm was flushed with saline solution.
Intraoperative vessel-flow measurements were made
using a perivascular microflow probe and mean flow readings were continuously displayed in millimeters per minute on the flowmeter console (Model HT300 Series; Transonic Systems, Ithaca, NY, USA). Prior to temporarily
clipping, flow within the three segments of MCA was all
measured. Baseline flows in the M1, superior M2 and inferior M2 segments were 26.7, 32.4 and 22.8 ml/minute,
respectively (Table). The aneurysm was then reconstruct-

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Fig 5. Frontal (A) and lateral (B) postoperative angiogram confirming complete obliteration of the aneurysm
with preservation of the MCA.

Fig 6. Schematic illustration of the ultrasonic transit-time principle.

ed with three clips. This allowed a complete occlusion of
the aneurysm. Flow within MCA was redemonstrated using
the microvascular ultrasonic flow probe after the temporary clips were removed. One of the branches was found
having no flow in it. By readjusting the clips multiple times, flow within all MCA segments was able to be preserved, particularly in the inferior M2 segment (Graphic).
The aneurysm was found to be well occluded with no evidence of leakage. After clip readjustment, flow in the M1
segment was normal and flow in the inferior M2 decreased to 12.6 ml/minute (Fig 4A), whereas flow in the
superior M2 increased to 43.6 ml/minute, indicating that
there was a compensatory increase in response to the reduced inferior M2 flow. It is important to note that, based
on visual inspection alone, the surgeon had been satisfied
with the clip placement. It was the low flow reading in
the MCA segments that prompted the surgeon to adjust
the clip (Fig 4. B). Postoperative angiography confirmed
complete obliteration of the aneurysm with preservation
of the afferent vessel (Fig 5A and B). The patient has had
a good outcome with no focal ischemic deficit postsurgery.

DISCUSSION
The goals of aneurysm surgery are to eliminate
the aneurysm from the intracranial circulation and
to maintain the patency of normal vessels. Traditionally, verification of these goals has been provided by observation with the use of an operating microscope. It is well recognize that visual inspection
of the clip alone or audio Doppler signals used to
detect flow compromise during aneurysm surgery
are subjective methods that can be inadequate or
misleading some cases. It is not always possible to
visualize fully the area encompassed by the clip. Likewise, flow velocities increase in the presence of
stenosis and thus a strong Doppler signal may, in fact,
be associated with a reduction in lumen diameter
and a decrease in blood flow.
Angiography is considered the gold standard
for assessing vessel-flow compromise after aneurysm
clipping, but it is not performed routinely at most

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graphy in 40 consecutive patients harboring 54 aneurysms, 52 of which were clipped. Intraoperative angiography prompted clip adjustment in 18 (34%) of
the 52 aneurysms. Twenty-two percent of these clip
adjustments were due to parent artery stenosis, 44%
for residual aneurysm, and 33% for both. Eighty-eight
percent of the clip adjustments were necessary on large or giant aneurysms. In addition, the authors found
that aneurysms located at anatomical sites with multiple inflow and distal outflow vessels and midline,
deep, and ophthalmic lesions had a highly significant
association with clip adjustment.
Graphic. Mean blood flow measuments (ml/min) within inferior M2 segment of MCA demonstrated using de microvascular flow probe during aneurysm clipping and after multiple clip
readjusment.

Table 1. Blood flow within MCA demonstrated using de
microvascular flow probe.
MCA segment

M1

M2 superior

M2 inferior

Baseline
After coil and temporary
clip removal
After clip adjustment
Final value after multiple
clip adjustment

26.7

32.4

22.8

11.0
17.6

24.4
40.1

0.2
0

26.0

43.6

12.6

institutions. The equipment and personnel are not
universally available and the technique is expensive and time consumig8. Furthermore, the delay in
obtaining information about blood flow may be
unacceptable and the complication rate of angiography is by no means negligeble (1.7 to 2.9%)8,9.
Nevertheless, several studies have documented
the rates of vessel occlusion or clip adjustment based
on angiographic findings5-7,10,11. In a series of 66 patients who underwent postoperative angiography,
Macdonald et al.5 reported that there were unexpected stenosis in nine out of 78 (11.5%) patients,
resulting in six strokes and two deaths (10.3%). Futhermore, in the same study there was a 4% incidence of unexpected residual aneurysm and an additional 4% incidence of completely unclipped aneurysms. In a subsequent study, routine intraoperative angiography revealed an unsuspected arterial occlusion or residual aneurysm, leading to clip adjustment in 11 % of cases10.
Origitano et al.6 reported on the rate of clip adjustment made on the basis of intraoperative angio-

Derdeyn et al11., also demonstrated that the frequency of clip adjustment is associated with the size
and location of the aneurysm. In their series, intraoperative angiography prompted clip adjustment in
46 (16.8%) of 273 patients. The highest rates of clip
adjustment occurred in aneurysms of the superior hypophyseal artery (38.9%), superior cerebellar
artery (60%), and internal carotid bifurcation (33.3%),
suggesting that aneurysms in these locations warrant more intensive monitoring to avoid vascular
compromise. In another study, Payner et al7. reported that intraoperative angiography, when used selectively based on the surgeon’s concern about possible vessel stenosis branch occlusion, or residual
aneurysm, led to immediate repositioning of the
aneurysm clip in 27% of cases. Bailes et al.1 investigated 35 patients who underwent surgery for the
treatment of 42 cerebral aneurysms using a microvascular Doppler ultrasonography. They found an
incidence of 31% for unexpected stenosis of adjacent arteries.
The flow probe uses ultrasound transit-time technology to measure blood flow. The body of the
probe houses two piezoelectrical crystals that alternatively transmit and receive an ultrasonic signal in
both upstream and downstream directions with respect to the flow of blood (Fig 6). Using wide-beam illumination, the two transducers pass ultrasonic signals back and forth, alternately intersecting the vessel in upstream and downstream, directions. The flowmeter measures the “transit time” it takes for a wave
of ultrasound to travel the fixed distance from one
transducer to the other. The difference between the
upstream and downstream integrated transit times
is a measure of volume flow. The vessel is placed within a beam that fully and evenly illuminates the entire
blood vessel and the transit time of the wide beam
becomes a function of the volume flow intersecting
the beam, independent of vessel dimensions.

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The ultrasonic beam intersects the vessel twice
on its reflective pathway. During each intersection,
the transit time of the beam is modified by a vector component of the flow. The full beam senses the
sum of these two vector components, that is, the
flow itself. If the angle of the beam is changed with
respect to the flow, one vector component of the
flow becomes greater and the second vector component diminishes, with little consequence to their
sum. The accuracy of the transit-time method of
blood volume flow measurement has been extensively validated12-16.
Quantitative flow measurements facilitate optimal clip placement by providing immediate verification that flow in the parent vessel and distal outflow branches are fully preserved. Obviously, repositioning the clip has inherent risks. If vessel stenosis or occlusion is suspected, the microflow probe
is very helpful in confirming flow integrity and avoiding unnecessary adjustments. In addition to assessing flow integrity in the parent vessel and distal branches after aneurysm clipping, we have found as
Nakayama et al.17, the microflow probe to be useful for measuring residual flow and collateral supply during temporary clipping or aneurysm trapping, and for evaluating the patency of extracranalintracranial bypasses. The limitation of perivascular ultrasound transit-time flow probe relate to the
inability to detect aneurysmal rests or residual neck.
A subject of interest to future investigations is to determine the values of mean blood flow reduction
which is of physiological relevance and when it is necessary to adjust the clip placement.
In conclusion, the ultrasound transit-time flow
probe provides objective, non-invasive cerebral blood flow measurements in real time in the parent
single-vessel and distal outflow branches intraoperatively during cerebral aneurysm surgery. In cases in which vessel-flow compromise is detected, the
clip can be repositioned within a few minutes, re-

sulting in immediate improvement in blood flow
and minimal ischemic time. The ultrasonic perivascular micro-flow probe can be useful tool in the management of intracranial aneurysms.
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